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Synaptic circuitry of serotonin-synthesizing and serotonin-accumulating amacrine cells in the retina of the cane toad, Bufo marinus

Published online by Cambridge University Press:  02 June 2009

Bao-Song Zhu ,
Charles Straznicky  and
Ian Gibbins
Bao-Song Zhu
Affiliation:
Department of Anatomy and Histology and Centre for Neuroscience, School of Medicine, The Flinders University of South Australia, Adelaide, Australia
Charles Straznicky
Affiliation:
Department of Anatomy and Histology and Centre for Neuroscience, School of Medicine, The Flinders University of South Australia, Adelaide, Australia
Ian Gibbins
Affiliation:
Department of Anatomy and Histology and Centre for Neuroscience, School of Medicine, The Flinders University of South Australia, Adelaide, Australia
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Abstract

The synaptic connections of amacrine cells synthesizing or accumulating serotonin in the retina of the cane toad, Bufo marinus, were studied by using preembedding double-labeling electron-microscopic immunocytochemistry. The binding sites of an anti-serotonin antibody were revealed by the diaminobenzidine reaction, whilst a colloidal gold-conjugated secondary antibody was used to detect an antibody to phenylalanine hydroxylase. Since the latter antibody recognizes tryptophan 5-hydroxylase, one of the synthesizing enzymes for serotonin, as well as tyrosine hydroxylase, the rate-limiting enzyme for catecholamine synthesis, the double labeling of the present study enabled us to identify three groups of labeled profiles at the ultrastructural level. The profiles of serotonin-synthesizing amacrine cells contained both diaminobenzidine reaction product and colloidal gold particles, whilst those of serotonin-accumulating and dopaminergic amacrine cells contained only diaminobenzidine reaction product or colloidal gold particles, respectively. The synapses of serotonin-synthesizing or serotonin-accumulating amacrine cells were distributed all through the inner plexiform layer of the retina. The profiles of serotonin-synthesizing amacrine cells predominantly received synapses from, and made synapses onto, unlabeled amacrine cell dendrites. They also received synapses from, and made synapses onto, bipolar cell terminals. They also made synapses onto presumed ganglion cell dendrites. However, the profiles of serotonin-accumulating cells made synapses only with unlabeled amacrine cell processes. There were close contacts between the profiles of serotonin-synthesizing and serotonin-accumulating amacrine cells. No synaptic relationships were observed between dopaminergic and serotonin-synthesizing or serotonin-accumulating amacrine cells. These observations indicate that serotonin-synthesizing amacrine cells and serotonin-accumulating amacrine cells in the retina of Bufo marinus are involved in different microcircuits in visual information processing.

Keywords

UltrastructureAmacrine cellsSerotoninRetinaAmphibian
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 1 , January 1995 , pp. 11 - 19
Copyright
Copyright © Cambridge University Press 1995

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References

Adolph, A.R. (1989). Pharmacological actions of peptides and indole-amines on turtle retinal ganglion cells. Visual Neuroscience 3, 411–423.CrossRefGoogle Scholar
Basbaum, A.I. (1989). A rapid and simple silver enhancement procedure for ultrastructural localization of the retrograde tracer WGA apo HRP-Av and its use in double-label studies with post-embedding immunocytochemistry. Journal of Histochemistry and Cytochemistry 37, 1811–1815.CrossRefGoogle ScholarPubMed
Bruun, A., Ehinger, B. & Sytsma, V.M. (1984). Neurotransmitter localization in the skate retina. Brain Research 295, 233–248.CrossRefGoogle ScholarPubMed
Chan, J., Aoki, C. & Pickel, V.M. (1990). Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. Journal of Neuroscience Methods 33, 113–127.CrossRefGoogle ScholarPubMed
Ehtnger, B. (1983). Functional role of dopamine in the retina. Progress of Retinal Research 3, 213–232.CrossRefGoogle Scholar
Ehtnger, B. & Florén, I. (1978). Quantitation of the uptake of indole-amines and dopamine in the rabbit retina. Experimental Eye Research 26, 1–11.CrossRefGoogle Scholar
Ehinger, B. & Holmgren, I. (1979). Electron microscopy of the indoleamine-accumulating neurons in the retina of the rabbit. Cell Tissue Research 197, 175–194.CrossRefGoogle ScholarPubMed
Eldred, W.D., Zucker, C., Karten, H.J. & Yazulla, S. (1983). Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. Journal of Histochemistry and Cytochemistry 31, 285–292.CrossRefGoogle ScholarPubMed
Frederick, J.M., Rayborn, M.E. & Hollyheld, J.G. (1989). Serotoninergic neurons in the retina of Xenopus laevis: Selective staining, identification, development, and content. Journal of Comparative Neurology 281, 516–531.CrossRefGoogle ScholarPubMed
Gábriel, R., Zhu, B.-S. & Straznicky, C. (1993). Synaptic contacts of serotonin-immunoreactive and 5,7-dihydroxytryptamine-accumulating neurons in the anuran retina. Neuroscience 54, 1103–1114.CrossRefGoogle Scholar
Gläsener, G., Schmidt, C. & Himstedt, W. (1988). Two populations of serotonin-immunoreactive neurons in the frog (Rana esculenta) retina. Neuroscience Letters 84, 251–254.CrossRefGoogle ScholarPubMed
Haan, E.A., Jennings, I.G., Cuello, A.C., Nakata, H., Fujisawa, H., Chow, C.W., Kushinsky, R., Brittingham, J. & Cotton, R.G.H. (1987). Identification of serotonergic neurons in human brain by a monoclonal antibody binding to all three aromatic amino acid hydroxylases. Brain Research 426, 19–27.CrossRefGoogle ScholarPubMed
Holmgren-Taylor, I. (1982). Electron microscopical observations on the indoleamine-accumulating neurons and their synaptic connections in the retina of the cat. Journal of Comparative Neurology 208, 144–156.CrossRefGoogle ScholarPubMed
Hurd, L.B. & Eldred, W.D. (1993). Synaptic microcircuitry of bipolar and amacrine cells with serotonin-like immunoreactivity in the retina of the turtle, Pseudemys scripta elegans. Visual Neuroscience 10, 455–472.CrossRefGoogle ScholarPubMed
Llewellyn-Smith, I.J., Song, Z-M., Costa, M., Bredt, D.S. & Snyder, S.H. (1992). Ultrastructural localization of nitric oxide syn-thase immunoreactivity in quinea-pig enteric neurons. Brain Research 577, 337–342.CrossRefGoogle Scholar
Marc, R.E., Liu, W.-L. S., Scholz, K. & Muller, J.F. (1988). Serotonergic and serotonin-accumulating neurons in the goldfish retina. Journal of Neuroscience 8, 3427–3450.CrossRefGoogle ScholarPubMed
Massey, S.C. & Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress of Neurobiology 28, 55–96.CrossRefGoogle ScholarPubMed
Millar, T.J. & Morgan, I.G. (1989). Serotonergic cells in the chicken retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 445–453. Berlin: Springer.CrossRefGoogle Scholar
Millar, T.J., Winder, C., Ishimoto, I. & Morgan, I.G. (1988). Putative serotonergic bipolar and amacrine cells in the chicken retina. Brain Research 439, 77–87.CrossRefGoogle ScholarPubMed
Mitchell, C.K. & Redburn, D.A. (1985). Analysis of pre- and post-synaptic factors of the serotonin system in rabbit retina. Journal of Cell Biology 100, 64–73.CrossRefGoogle Scholar
Osborne, N.N. (1980). In vitro experiments on the metabolism, uptake and release of 5-hydroxytryptamine in bovine retina. Brain Research 184, 283–297.CrossRefGoogle Scholar
Osborne, N.N. (1982). Evidence for serotonin being a neurotransmitter in the retina. In Biology of Serotonergic Transmission, ed. Osborne, N.N., pp. 401–430. Chichester, England: John Wiley & Sons.Google Scholar
Osborne, N.N. (1984). Indoleamines in the eye with special reference to the serotoninergic neurons of the retina. Progress of Retinal Research 4, 61–103.CrossRefGoogle Scholar
Osborne, N.N. (1988). Retinal serotonin and co-occurrence of serotonin with other neurotransmitters. In Neuronal Serotonin, ed. Osborne, N.N. & Hamon, M., pp. 129–148. New York, London: John Wiley & Sons.Google Scholar
Osborne, N.N. & Richardson, G. (1980). Specificity of serotonin uptake by bovine retina: Comparison with tryptamine. Experimental Eye Research 31, 31–39.CrossRefGoogle ScholarPubMed
Osborne, N.N., Nesselhut, T., Nicholas, D.A., Patel, S. & Cuello, C. (1982). Serotonin-containing neurons in the vertebrate retinas. Journal of Neurochemistry 39, 1519–1528.CrossRefGoogle ScholarPubMed
Parkinson, D. & Rando, R.R. (1981). Evidence for a neurotransmitter role for 5-hydroxytryptamine in chick retina. Journal of Neuroscience 1, 1211–1217.CrossRefGoogle ScholarPubMed
Sandell, J.H., Masland, R.H., Raviola, E. & Dacheux, R.F. (1989). Connections of indoleamine-accumulating cells in the rabbit retina. Journal of Comparative Neurology 283, 303–313.CrossRefGoogle ScholarPubMed
Schütte, M. & Witkovsky, P. (1990). Serotonin-like immunoreactivity in the retina of clawed frog Xenopus laevis. Journal ofNeurocytology 19, 504–518.CrossRefGoogle ScholarPubMed
Thomas, T.N. & Redburn, D. (1980). Serotonin uptake and release by subcellular fractions of bovine retina. Vision Research 20, 1–8.CrossRefGoogle ScholarPubMed
Watt, C.B. & Wilson, E.A. (1990). Synaptic organization of serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina. Neuroscience 35, 715–723.CrossRefGoogle ScholarPubMed
Weiler, R. & Ammenmüller, J. (1986). Immunocytochemical localization of serotonin in intracellularly analysed and dye-injected ganglion cells of the turtle retina. Neuroscience Letters 72, 147–152.CrossRefGoogle Scholar
Weiler, R. & Schütte, M. (1985). Morphological and pharmacological analysis of putative serotonergic bipolar and amacrine cells in the retina of turtle, Pseudemys scripta elegans. Cell Tissue Research 241, 373–382.CrossRefGoogle ScholarPubMed
Wilhelm, M., Zhu, B.-S., Gábriel, R. & Straznicky, C. (1993). Immunocytochemical identification of serotonin-synthesizing neurons in the vertebrate retina: A comparative study. Experimental Eye Research 56, 231–240.CrossRefGoogle ScholarPubMed
Yang, S.-Z., Lam, D.M.-K. & Watt, C.B. (1989). Localization of serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina. Journal of Comparative Neurology 287, 28–37.CrossRefGoogle Scholar
Young, H.M. & Vaney, D. (1990). The retinae of prototherian mammals possess neuronal types that are characteristic of nonmammalian retinae. Visual Neuroscience 5, 61–66.CrossRefGoogle Scholar
Zhu, B.-S. & Straznicky, C. (1990). Morphology and distribution of serotonin-like immunoreactive amacrine cells in the retina of Bufo marinus. Visual Neuroscience 5, 371–378.CrossRefGoogle ScholarPubMed
Zhu, B.-S. & Straznicky, C. (1992). Large serotonin-like immunoreactive amacrine cells in the retina of developing Xenopus laevis. Developmental Brain Research 69, 109–116.CrossRefGoogle ScholarPubMed
Zhu, B.-S., Gábriel, R. & Straznicky, C. (1992). Serotonin synthesis and accumulation by neurons in the anuran retina. Visual Neuroscience 9, 377–388.CrossRefGoogle ScholarPubMed